Abstract
In ostariophysan fish, the detection of alarm substance released from the skin of a conspecific or a sympatric heterospecific may elicit alarm reactions or antipredator behavioral responses. In this study, experiments were performed to characterize and quantify the behavioral response threshold of Leporinus piau, both individually and in schools, to growing dilutions of conspecific (CAS) and heterospecific skin extract (HAS). The predominant behavioral response to CAS stock stimulation was biphasic for fish held individually, with a brief initial period of rapid swimming followed by a longer period of immobility or reduced swimming activity. As the dilution of skin extract was increased, the occurrence and magnitude of the biphasic alarm response tended to decrease, replaced by a slowing of locomotion. Slowing was the most common antipredator behavior, observed in 62.5% of animals submitted to HAS stimulation. School cohesion, measured as proximity of fish to the center of the school, and swimming activity near the water surface significantly increased after exposure to CAS when compared with the control group exposed to distilled water. Histological analysis of the epidermis revealed the presence of Ostariophysi-like club cells. The presence of these cells and the behavioral responses to conspecific and heterospecific skin extract stimulation suggest the existence of a pheromone alarm system in L. piau similar to that in Ostariophysi, lending further support for the neural processing of chemosensory information in tropical freshwater fish.
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References
Barbosa Júnior A, Hoffmann A (2007) Alarm reaction in a South American teleost fish piauçu Leporinus macrocephalus. Comp Biochem Physiol, B 148:S39
Britski HA, Sato Y, Rosa ABS (1984) Manual de identificação de peixes da região de Três Marias, com chaves de identificação para peixes da Bacia do Rio São Francisco. Câmara dos Deputados/CODEVASF, Brasília
Brown GE, Adrian JC, Naderi NT, Harvey MC, Kelly JM (2003) Nitrogen oxides elicit antipredator responses in juvenile channel catfish, but not in convict cichlids or rainbow trout: conservation of the ostariophysan alarm pheromone. J Chem Ecol 29:1781–1796
Brown GE, Adrian JC, Shih ML (2001) Behavioral responses of fathead minnows to hypoxanthine-3-N-oxide at varying concentrations. J Fish Biol 58:1465–1470
Brown GE, Adrian JC, Smyth E, Leet H, Brennan S (2000) Ostariophysan alarm pheromones: laboratory and field tests of the function significance of nitrogen oxides. J Chem Ecol 26:139–154
Chivers DP, Wisenden BD, Hindman CJ et al (2007) Epidermal ‘alarm substance’ cells of fishes are maintained by non-alarm functions: possible defence against pathogens, parasites and UVB radiation. Proc R Soc B 274:2611–2619
Chivers DP, Smith RJF (1994) Fathead minnows, Pimephales promelas, acquire predator recognition when alarm substance is associated with the sight of unfamiliar fish. An Behav 48:597–605
Chivers DP, Smith RJF (1998) Chemical alarm signalling in aquatic predator–prey systems: a review and prospectus. Écoscience 5:338–352
Ferrari MCO, Chivers DP (2006) Learning treat-sensitive predator avoidance: how do fathead minnows incorporate conflicting information? An Behav 71:19–26
Figueroa RI, Rodríguez-Sabarís R, Aldegunde M, Soengas JL (1975) Effects of food deprivation on 24-h changes in brain and liver carbohydrate and ketone body metabolism of rainbow trout. J Fish Biol 161:125–142
Von Frisch K (1938) Zur psychologie des fisch-schwarmes. Naturwissenschaften 26:601–606
Gerlai R, Fernandes Y, Pereira T (2009) Zebrafish (Danio rerio) responds to the animated image of a predator: towards the development of an automated aversive task. Behav Brain Res 201:318–324
Giaquinto PC, Volpato GL (2005) Chemical cues related to conspecific size in pintado catfish, Pseudoplatystoma coruscans. Acta Ethol 8:65–69
Godinho HP, Godinho AL (2003) Águas, peixes e pescadores do São Francisco das Minas Gerais. PUCMinas, Belo Horizonte
Halbgewachs CF, Marchant TA, Kusch RC, Chivers DP (2009) Epidermal club cells and the innate immune system of minnows. Biol J Linn Soc 98:891–897
Heczko EJ, Seghers BH (1981) Effects of alarm substance on schooling in the common shinner (Notropis comutus, Cyprinidae). Environ Biol Fish 6:25–29
Hoare DJ, Couzin ID, Godin J‐GJ, Krause J (2004) Context‐depende group size choice in fish. An Behav 67:155–164
Hobson ES (1968) Predatory behavior of some inshore fishes in the Gulf of California. Copeia 73:1–92
Ide LM, Urbinati EC, Hoffmann A (2003) The role of olfaction in the behavioral and physiological responses to conspecific skin extract in Brycon cephalus. J Fish Biol 63:332–343
Jachner A (1996) Alarm reaction in bleak (Alburnus alburnus (L.), Cyprinidae) in response to chemical stimuli from injured conspecifics. Hydrobiologia 325:151–155
Kats LB, Dill LM (1998) The scent of death: chemosensory assessment of predation risk by prey animals. Écoscience 5:361–394
Kelly JM, Adrian JC, Brown GE (2006) Can the ratio of aromatic skeletons explain cross-species responses within evolutionarily conserved Ostariophysan alarm cues?: testing the purine-ratio hypothesis. Chemoecology 16:93–96
Klemm WR (2001) Behavioral arrest: in search of the neural control system. Prog Neurobiol 65:453–471
Lawrence BJ, Smith RJF (1989) Behavioral response of solitary fathead minnows, Pimephales promelas, to alarm substance. J Chem Ecol 15:209–218
Lopez CM, Alvim MC (1997) Larviculture of surubim Pseudoplatystoma coruscans Agassiz, 1829 (Siluriformes: Pimelodidae) in laboratory: a preliminary study. In: Val AL (ed) Proceedings of the international symposium of biology of tropical fishes, Manaus, Amazon, Brazil, 1997
Mathis A, Smith RJF (1993) Intraspecific and cross-superoder responses to chemical alarm signals by brook stickleback. Ecology 74:2395–2404
Milinski M (1977) Experiments on the selection by predators against spatial oddity of their prey. Z Tierpsychol 43:311–325
Mirza RS, Chivers DP (2003) Fathead minnows learn to recognize heterospecific alarm cues they detect in the diet of a known predator. Behavior 140:1359–1369
Parra KV, Adrian JC Jr, Gerlai R (2009) The synthetic substance hypoxanthine 3-N-oxide elicits alarm reactions in zebrafish (Danio rerio). Behav Brain Res 205:336–341
Pfeiffer W (1963) Alarm substances. Experientia 19:113–123
Pfeiffer W (1977) The distribution of fright reaction and alarm substance cells in fishes. Copeia 1977:653–665
Pfeiffer W, Riegelbauer G, Meier G, Scheibler B (1985a) Effect of hypoxanthine-3-N-oxide and hypoxanthine-1-N-oxide on central nervous excitation of the black tetra, Gymnocorymbus ternetzi (Characidae, Ostariophysi, Pisces) indicated by dorsal light dorsal response. J Chem Ecol 11:507–523
Pfeiffer W, Walz U, Wolf R, Mangold-Wernado U (1985b) Effects of steroid hormones and other substances on alarm substance cells and mucous cells in the epidermis of the European minnow, Phoxinus phoxinus (L.), and other Ostariophysi (Pisces). J Fish Biol 27:553–570
Reebs SC (2002) Plasticity of diel and circadian activity rhythms in fishes. Rev Fish Biol Fish 12:349–371
Schutz F (1956) Vergleichende untersuchungen über die schreckreaktion bei fischen und derenverbreitung. J Comp Physiol Biochem A 38:84–135
Smith RJF (1992) Alarm signals in fishes. Rev Fish Biol Fish 2:33–63
Smith ME (2000) Alarm response of Arius felis to chemical stimuli from injured conspecifics. J Chem Ecol 26:1635–1647
Solomon DJ (1977) A review of chemical communication in freshwater fish. J Fish Biol 11:363–376
Speedie N, Gerlai R (2008) Alarm substance induced behavioral responses in zebrafish (Danio rerio). Behav Brain Res 188:168–177
Verheijen FJ (1956) Transmission of a flight reaction amongst a school of fish and the underlying sensory mechanisms. Experientia 12:202–204
Wisenden BD (2008) Active space of chemical alarm cue in natural minnow populations. Behaviour 145:391–407
Wisenden BD, Barbour KA (2005) Antipredator responses to skin extract of redbelly dace by free-ranging populations of redbelly dace and fathead minnows. Environ Biol Fish 72:227–233
Wisenden BD, Chivers DP, Brown GE, Smith RJF (1995) The role of experience in risk assessment: avoidance of areas chemically labeled with fathead minnow alarm pheromone by conspecifics and heterospecifics. Écoscience 2:116–122
Zar JH (1996) Biostatistical Analysis, 3rd edn. Prentice-Hall, New Jersey
Acknowledgements
Part of this research was a portion of the undergraduate research projects and scientific initiation of A.B.J. and E.J. M. at the Universidade Federal de São João del‐Rei. The authors would like to thank Mr. Rubens Fernando de Melo for the technical support in the histological procedures and the Commercial Supplier of fish GMAlevinos for donating the L. piau. This research was financially supported by Fundação de Amparo a UFSJ (FAUF), Fundação de Amparo a Pesquisa do Estado de Minas Gerais (FAPEMIG), UFSJ, and FMRP/USP.
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Barbosa Júnior, A., Magalhães, E.J., Hoffmann, A. et al. Conspecific and heterospecific alarm substance induces behavioral responses in piau fish Leporinus piau . acta ethol 13, 119–126 (2010). https://doi.org/10.1007/s10211-010-0081-6
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DOI: https://doi.org/10.1007/s10211-010-0081-6